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Aghdashloo began acting in Iran in the late 1970s before departing during the Iranian Revolution. Her breakthrough role came in 2003's House of Sand and Fog, for which she received a nomination for the Academy Award for Best Supporting Actress. Two years later, she guest-starred in season four of 24, and in 2006 she appeared in X-Men: The Last Stand with Patrick Stewart, Kelsey Grammer and Famke Janssen. In 2008 she won a Primetime Emmy Award for Outstanding Supporting Actress in a Miniseries or Movie for her portrayal of Sajida Talfah in the BBC docudrama House of Saddam; she also guest-starred on The Simpsons, voicing Mina, one of the show's first Muslim characters.

In an episode of Law & Order: Special Victims Unit first airing in 2011, she played a detective inspector with the Brooklyn District Attorney's office, Saliyah "Sunny" Qadri, who interferes with what is technically a Manhattan (New York County) crime scene (the death of a colleague from the office). She also appeared in an episode of the CBS Television Studios series NCIS as one of a family who arrives in America, only to be detained on the ship for most of the episode (and therefore not on American soil).

In 2014, she appeared in Jon Stewart's directorial debut Rosewater, a biopic of Maziar Bahari. Aghdashloo has a lead role as Chrisjen Avasarala on the Syfy series The Expanse, which began in 2015.